Descriptive urological record of chimpanzees (Pan troglodytes) in the wild and limitations associated with using multi-reagent dipstick test strips

Ten urine chemistry parameters were measured on 74 voided urine samples from 34 wild chimpanzees (Pan troglodytes). Multi-reagent urine dipstick tests were performed and results determined using colorimetric scales. Urine pH measured between 8 and 9 units in 91% of the chimpanzees. Test pads detected protein, erythrocytes, leukocyte esterase activity, and nitrites, ketones and bilirubin in 47, 32, 29, and <10% of the chimpanzees, respectively. No apparent association between positive test results for blood in adult females and reproductive status was found. Overall, 17 of the 34 chimpanzees had positive urine test results for protein, hemoglobin, erythrocytes, leukocytes, nitrites, ketones, and/or bilirubin. Dipstick urinalysis alone is an unreliable method for assessing health and physiological status of wild chimpanzees. However, if combined with other diagnostics it could prove to be a valuable health-monitoring tool. Limitations associated with this methodology need to be considered when interpreting urinary dipstick test results.     

Female Coalitions Against Male Aggression in Wild Chimpanzees of the Budongo Forest

In the wild, female chimpanzees (Pan troglodytes) are subject to male aggression that at times can be prolonged or particularly violent. There are no reports of cooperative retaliation to such aggression, a strategy observed in the congeneric Pan paniscus, from the wild despite >4 decades of detailed behavioral study across a number of populations and its occurrence among captive female chimpanzees. If the reports from captivity represent an inherent capacity, then the absence of similar reports from wild populations suggests that females may be able to form coalitions only under appropriate ecological and demographic conditions. During a study of male and female aggressive interactions among chimpanzees of the Budongo Forest, Uganda, wild adult female chimpanzees sometimes formed coalitions with one another to retaliate against male aggression. This may be possible because these females tend to be more gregarious than in other populations of East African chimpanzees, as other studies of the same population have suggested; the extent and variation of female chimpanzee social strategies may, therefore, need reconsideration. Further, my observations strengthen the argument that at least some of the differences between chimpanzees and bonobos may be more of degree than of kind.     

Evidence for a complex demographic history of chimpanzees

To characterize patterns of genomic variation in central chimpanzees(Pan troglodytes troglodytes) and gain insight into their evolution,we sequenced nine unlinked, intergenic regions, representinga total of 19,000 base pairs, in 14 individuals. When theseDNA sequences are compared with homologous sequences previouslycollected in humans and in western chimpanzees (Pan troglodytesverus), nucleotide diversity is higher in central chimpanzeesthan in western chimpanzees or in humans. Consistent with alarger effective population size of central chimpanzees, levelsof linkage disequilibrium are lower than in humans. Patternsof linkage disequilibrium further suggest that homologous geneconversion may be an important contributor to genetic exchangeat short distances, in agreement with a previous study of thesame DNA sequences in humans. In central chimpanzees, but notin western chimpanzees, the allele frequency spectrum is significantlyskewed towards rare alleles, pointing to population size changesor fine-scale population structure. Strikingly, the extent ofgenetic differentiation between western and central chimpanzeesis much stronger than what is seen between human populations.This suggests that careful attention should be paid to geographicsampling in studies of chimpanzee genetic variation.     

Chimpanzees as an outgroup for the examination of human dental evolution

In the assessment of human origins, chimpanzees (Pan troglodytes, henceforth called Pan) represent the best hominoid outgroup for comparisons. Such an outgroup roots the "anatomically modern" human population cluster, or continuum. This study incorporates chimpanzees into a worldwide modern human database of quantified complete tooth variables (approximately 30 per tooth; e.g., root, pulp, enamel) in an attempt to develop a more accurate phylogeny of the hominoid continuum, with only intervening extinct hominids missing. Canonical discriminate analysis was performed mainly among Liberian common chimpanzees and global samples of humans. The first canonical variable explained 70% of the total variance and showed a tight cluster of humans, with chimpanzees as a distant outgroup. Within the human community, first non-San Bushman, sub-Saharan Africans and Andamanese, and then, close in, Australian aborigines were positioned towards Pan. Their relative orientation suggested an African human origin with the first branch within sub-Saharan Africa: sub-Saharan Africans and San Bushmen. Next, Andamanese Negritos, and then Australian aborigines, formed the early first surviving modern human lineage to leave Africa. Thin enamel and big teeth with relatively large roots characterized Pan nonmolar teeth. Humans showed a generalized sexual dimorphism for all teeth, with males having bigger teeth, bigger relative roots, and thinner enamel than females, while only Pan canines had significant and impressive sexual dimorphism. Interestingly, Pan molars were not larger than human molars. The data suggest that although hominids underwent two dental macroevolutionary events, the lineage leading to modern humans only experienced anterior tooth-size reduction. The suggested evolutionary significance of the observed total tooth variation is discussed.     

Body size and proportions in chimpanzees,with special reference toPan troglodytes schweinfurthii from Gombe National Park,Tanzania

Body weight, cranial capacity, linear and joint area data from ten free-ranging adult chimpanzees from Gombe National Park, Tanzania with known life histories allow study of variation in a local population and comparison to other populations ofPan troglodytes and toPan paniscus. Because individuals in the Gombe population are small compared to other common chimpanzees, they provide a useful comparison toPan paniscus. Body weight and some linear dimensions overlap withPan paniscus. However, cranial capacity, tooth size, and body proportions of Gombe individuals lie within the range of otherPan troglodytes and are distinct fromPan paniscus.     

Spatiotemporal Variation in Bonobo (Pan paniscus) Habitat Use in a Forest–Savanna Mosaic

International Journal of Primatology - Understanding the ecological and behavioral variation of primates is central to improving conservation strategies. Studies of chimpanzees (Pan troglodytes)...     

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Behavioral diversity in populations of free-ranging chimpanzees in Africa: is it culture?

Behavioral differences exist among populations of wild chimpanzees (Pan troglodytes, Hominoidea) across Africa. Deciding if these are cross-cultural differences demands careful interpretation and rigorous scrutiny. Even standard patterns like social grooming may show variation in detail between neighboring populations. Some patterns of tool use, such as using hammers to crack nuts, also vary across far western Africa. At least 37 populations of free-ranging chimpanzees show tool use, and 14 show at least one habitual pattern of tool use. Regional differences exist among the three subspecies or geographical races of chimpanzees. Convincing empirical demonstration of social customs and traditions in non-human species is problematical, and even something so simple in principle as innovation is hard to show in practice. However, culture need not depend on imitation, teaching, or language, either in humans or in other species.     

Comparative nuclear and mitochondrial genome diversity in humans and chimpanzees

Restriction mapping and sequencing have shown that humans have substantially lower levels of mitochondrial genome diversity (d) than chimpanzees. In contrast, humans have substantially higher levels of heterozygosity (H) at protein-coding loci, suggesting a higher level of diversity in the nuclear genome. To investigate the discrepancy further, we sequenced a segment of the mitochondrial genome control region (CR) from 49 chimpanzees. The majority of these were from the Pan troglodytes versus subspecies, which was underrepresented in previous studies. We also estimated the average heterozygosity at 60 short tandem repeat (STR) loci in both species. For a total sample of 115 chimpanzees, d = 0.075 +/0 0.037, compared to 0.020 +/- 0.011 for a sample of 1,554 humans. The heterozygosity of human STR loci is significantly higher than that of chimpanzees. Thus, the higher level of nuclear genome diversity relative to mitochondrial genome diversity in humans is not restricted to protein-coding loci. It seems that humans, not chimpanzees, have an unusual d/H ratio, since the ratio in chimpanzees is similar to that in other catarrhines. This discrepancy in the relative levels of nuclear and mitochondrial genome diversity in the two species cannot be explained by differences in mutation rate. However, it may result from a combination of factors such as a difference in the extent of sex ratio disparity, the greater effect of population subdivision on mitochondrial than on nuclear genome diversity, a difference in the relative levels of male and female migration among subpopulations, diversifying selection acting to increase variation in the nuclear genome, and/or directional selection acting to reduce variation in the mitochondrial genome.      

Ontogeny of body size variation in African apes

Size variation in African apes (Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) is substantial, both within and between species. We investigate the possible evolutionary significance of this variation through an analysis of the ontogeny of size variation in this group. In addition, we highlight possible areas of future endocrinological research, and evaluate recently proposed alternative models that attempt to account for ontogenetic variation in apes. The present study shows that intergeneric variation in size is largely a consequence of differences among species in the rate of body weight growth. Interspecific size variation in Pan is a product of both rate and duration differences in growth. The ontogenetic bases of sexual dimorphism vary in this group. Dimorphism is largely a result of sex differences in the duration of body weight growth in gorillas and pygmy chimpanzees, but results from differences in the rate of growth in common chimpanzees. Ontogenetic analyses largely confirm earlier interpretations, but with better data and methods. The great degree of ontogenetic variation within and among these species, especially in the timing and magnitude of “pubertal” growth spurts, implies that studies of endocrine growth control in African apes could be a productive line of future research. We also suggest that ontogenetic variation can be understood with respect to ecological risks. Growth rates seem to be negatively correlated with ecological risk in African apes, suggesting links between ontogenetic patterns and social and ecological variables. High growth rates in gorillas compared to Pan are most consistent with this model. Variation between chimpanzees and pygmy chimpanzees (especially females) also seem to fit predictions of this model. © 1996 Wiley-Liss, Inc.     

Genetic Sampling of Unhabituated Chimpanzees (Pan troglodytes schweinfurthii) in Gishwati Forest Reserve, an Isolated Forest Fragment in Western Rwanda

Many primate populations currently live in forest fragments. These populations are often unhabituated, elusive, and contain few individuals, making them difficult to study through direct observation. Noninvasive genetic methods are useful for surveying these unhabituated populations to infer the number and sex of individuals and the genetic diversity of the population. We conducted genetic analysis on 70 fecal samples from eastern chimpanzees (Pan troglodytes schweinfurthii) in Gishwati Forest Reserve, a forest fragment in western Rwanda. We genotyped all but two of these samples using 12 autosomal and 13 Y-chromosome microsatellite markers previously used in analyses of other chimpanzee populations. The genetic data show that these samples represent a minimum of 19 individuals (7 females, 12 males). However, because we may not have sampled all individuals in the population, we also performed mark-recapture analysis with the genetic data and found that the entire population likely numbers between 19 and 29 individuals. These results are consistent with opportunistic observations of at least 19 individual chimpanzees. Levels of variation at the Y-chromosome microsatellites were similar to those observed in other chimpanzee communities, suggesting that the chimpanzees in this forest are members of a single community. These results provide a baseline count of the number of male and female chimpanzees in the Gishwati Forest Reserve, and the data provide the potential for follow-up studies aimed at tracking individuals over time, thus aiding conservation management of this unhabituated population.     

Comparative Feeding Ecology of Two Communities of Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) in Kibale National Park,Uganda

Several recent studies have documented considerable intraspecific and intrapopulation ecological variation in primates. However, we generally lack an understanding of how such variability may be linked to concomitant demographic variation among groups or populations of the same species, particularly in regard to large-bodied and wide-ranging species with high ecological flexibility, such as chimpanzees (Pan troglodytes). We compared the feeding ecology of chimpanzees inhabiting 2 sites in Kibale National Park, Uganda that differ 3-fold in chimpanzee density and support notably different plant communities. Chimpanzees at Ngogo, a site with the largest known chimpanzee community and unusually high chimpanzee density, spent a significantly lower percentage of time resting (and pregnant and lactating females spent more time feeding), incorporated higher percentages of ripe fruit in their diet, had lower dietary diversity values, and had shorter and less variable average patch residency times than did their counterparts at the nearby Kanyawara site, which supports a relatively low density of chimpanzees. In addition, feeding party size was significantly and positively related to feeding patch size at Ngogo, but not at Kanyawara. Together these findings aid in explaining the noted disparity in chimpanzee community size and density between Ngogo and Kanyawara by suggesting that the diet of Ngogo chimpanzees is of higher overall quality than that of Kanyawara chimpanzees. They also highlight the potentially profound influence of even small-scale habitat heterogeneity on the ecology of primates. Researchers must take such influences into account when attempting to draw conclusions about species- or population-level characteristics.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5

Human immunodeficiency virus type 1 (HIV-1) evolved via cross-species transmission of simian immunodeficiency virus (SIVcpz) from chimpanzees (Pan troglodytes). Chimpanzees, like humans, are susceptible to infection by HIV-1. However, unlike humans, infected chimpanzees seldom develop immunodeficiency when infected with SIVcpz or HIV-1. SIVcpz and most strains of HIV-1 require the cell-surface receptor CC chemokine receptor 5 (CCR5) to infect specific leukocyte subsets, and, subsequent to infection, the level of CCR5 expression influences the amount of HIV-1 entry and the rate of HIV-1 replication. Evidence that variants in the 5' cis-regulatory region of CCR5 (5'CCR5) affect disease progression in humans suggests that variation in CCR5 might also influence the response of chimpanzees to HIV-1/SIVcpz. To determine whether patterns of genetic variation at 5'CCR5 in chimpanzees are similar to those in humans, we analyzed patterns of DNA sequence variation in 37 wild-born chimpanzees (26 P. t. verus, 9 P. t. troglodytes, and 2 P. t. schweinfurthii), along with previously published 5'CCR5 data from 112 humans and 50 noncoding regions in the human and chimpanzee genomes. These analyses revealed that patterns of variation in 5'CCR5 differ dramatically between chimpanzees and humans. In chimpanzees, 5'CCR5 was less diverse than 80% of noncoding regions and was characterized by an excess of rare variants. In humans, 5'CCR5 was more diverse than 90% of noncoding regions and had an excess of common variants. Under a wide range of demographic histories, these patterns suggest that, whereas human 5'CCR5 has been subject to balancing selection, chimpanzee 5'CCR5 has been influenced by a selective sweep. This result suggests that chimpanzee 5'CCR5 might harbor or be linked to functional variants that influence chimpanzee resistance to disease caused by SIVcpz/HIV-1.     

Bivariate and multivariate growth allometry: statistical and biological considerations

Bivariate and multivariate analyses of 55 cranial dimensions were completed on ontogenetic series of Pygmy chimpanzees ( Pan paniscus ), Common chimpanzees ( Pan troglodytes ), and gorillas ( Gorilla gorilla ). Subanalyses described here were specifically designed to compare and crosscheck quantitative assessments of relative growth as determined using the bivariate and multivariate (principal components analysis—PCA) approaches. Results indicate a strong concordance between the bivariate and multivariate patterns, empirically supporting the claim that PCA provides an effective multivariate approach to analysing growth allometry. Comparison of bivariate and multivariate results also suggests that in multi-group PCA, the first component summarizes shape variation resulting from the sharing and extension of common patterns of growth allometry, while the second and subsequent components summarize shape variation resulting from divergent growth trajectories, reflected in bivariate comparisons as either vertical shifts and/or slope differences. Examination of non-normalized first component loadings, plus a comparison with estimates of logarithmic growth in the cranial dimensions, reveals that the non-normalized loadings are proportional to coefficients of specific growth. This finding further links the bivariate and multivariate approaches, grounding both in Huxley's theoretical notions of multiplicative and relative growth.     

Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. Diet composition and diversity

Chimpanzees (Pan troglodytes) are ecologically flexible omnivores with broad diets comprising many plant and animal foods, although they mostly eat fruit (including figs). Like other ecologically flexible nonhuman primates (e.g., baboons, Papio spp.) with broad diets, their diets vary across habitats. Much data on diets come from short studies that may not capture the range of variation, however, and data are scant on variation within habitats and populations. We present data on diet composition and diversity for chimpanzees at Ngogo, in Kibale National Park, Uganda, collected over a 15-year period, with a focus on the plant components of the diet. We compare Ngogo data to those on chimpanzees at the nearby Kibale site of Kanyawara, on other chimpanzee populations, and on some other frugivorous-omnivorous primates. Results support the argument that chimpanzees are ripe fruit specialists: Ngogo chimpanzees ate a broad, mostly fruit-based diet, feeding time devoted to fruit varied positively with fruit availability, and diet diversity varied inversely with fruit availability. Comparison of Ngogo and Kanyawara shows much similarity, but also pronounced within-population dietary variation. Chimpanzees fed much more on leaves, and much less on pith and stems, at Ngogo. Figs accounted for somewhat less feeding time at Ngogo, but those of Ficus mucuso were quantitatively the most important food. This species is essentially absent at Kanayawara; its abundance and high productivity at Ngogo, along with much higher abundance of several other important food species, help explain why chimpanzee community size and population density are over three times higher at Ngogo. High inter-annual variation at Ngogo highlights the value of long-term data for documenting the extent of ecological variation among chimpanzee populations and understanding how such variation might affect population biology and social dynamics.     

Individual Variation in Behavioural Reactions to Unfamiliar Conspecific Vocalisation and Hormonal Underpinnings in Male Chimpanzees

It has been established that various species exhibit personality, defined as intra‐individual consistency and inter‐individual variation in behavioural phenotypes. For example, certain individuals may demonstrate consistently greater behavioural reactions and elevated stress responses. We conducted playback experiments and hormonal analyses on male chimpanzees (Pan troglodytes) in captivity to investigate the patterns and proximate mediators of individual variations in behavioural reactions. We found intra‐individual consistency and inter‐individual variation in behavioural reactions (intensive vigilance towards the direction of speakers) to vocalisations by unfamiliar chimpanzees. This behavioural reaction was positively correlated with changes in salivary cortisol concentration, suggesting that stress is a proximate factor mediating the variation in behavioural reactions. The males who were highly responsive to the conspecific vocalisation also exhibited high behavioural reactions towards the neutral broadcast stimulus (the jungle crow’s Corvus macrorhynchos ‘ka’ vocalisation). This observation is consistent with the notion that male chimpanzees vary in intrinsic behavioural tendency to different stimuli.     

Flexible and Persistent Tool-using Strategies in Honey-gathering by Wild Chimpanzees

Several populations of wild chimpanzees use tools to raid bee nests, but preliminary observations of chimpanzees in the Congo Basin indicate that they may have developed sophisticated technical solutions to gather honey that differ from those of apes in other regions. Despite the lack of habituated groups within the range of the central subspecies, there have been several reports of different types of tools used by chimpanzees to open beehives and gather honey. Researchers have observed some of these behaviors (honey dipping) in populations of western and eastern chimpanzees, whereas others (hive pounding) may be limited to this region. Toward evaluating hypotheses of regional tool using patterns, we provide the first repeated direct observations and systematic documentation of tool use in honey-gathering by a population of Pan troglodytes troglodytes. Between 2002 and 2006, we observed 40 episodes of tool use in honey-gathering by chimpanzees in the Goualougo Triangle, Republic of Congo. Pounding was the most common and successful strategy to open beehives. Chimpanzees at this site used several tools in a single tool-using episode and could also attribute multiple functions to a single tool. They exhibited flexibility in responses toward progress in opening a hive and hierarchical structuring of tool sequences. Our results support suggestions of regional tool using traditions in honey-gathering, which could be shaped by variation in bee ecology across the chimpanzee range. Further, we suggest that these chimpanzees may have an enhanced propensity to use tool sets that could be related to other aspects of their tool repertoire. Clearly, there is still much to be learned about the behavioral diversity of chimpanzees residing within the Congo Basin.     

Tolerance for inequity may increase with social closeness in chimpanzees

Economic decision-making depends on our social environment. Humans tend to respond differently to inequity in close relationships, yet we know little about the potential for such variation in other species. We examine responses to inequity in several groups of chimpanzees (Pan troglodytes) in a paradigm similar to that used previously in capuchin monkeys (Cebus apella). We demonstrate that, like capuchin monkeys, chimpanzees show a response to inequity of rewards that is based upon the partner receiving the reward rather than the presence of the reward alone. However, we also found a great amount of variation between groups tested, indicating that chimpanzees, like people, respond to inequity in a variable manner, which we speculate could be caused by such variables as group size, the social closeness of the group (as reflected in length of time that the group has been together) and group-specific traditions.     

How Abnormal Is the Behaviour of Captive,Zoo-Living Chimpanzees?

BACKGROUND: Many captive chimpanzees (Pan troglodytes) show a variety of serious behavioural abnormalities, some of which have been considered as possible signs of compromised mental health. The provision of environmental enrichments aimed at reducing the performance of abnormal behaviours is increasing the norm, with the housing of individuals in (semi-)natural social groups thought to be the most successful of these. Only a few quantitative studies of abnormal behaviour have been conducted, however, particularly for the captive population held in zoological collections. Consequently, a clear picture of the level of abnormal behaviour in zoo-living chimpanzees is lacking. METHODS: We present preliminary findings from a detailed observational study of the behaviour of 40 socially-housed zoo-living chimpanzees from six collections in the United States of America and the United Kingdom. We determined the prevalence, diversity, frequency, and duration of abnormal behaviour from 1200 hours of continuous behavioural data collected by focal animal sampling. RESULTS, CONCLUSION AND SIGNIFICANCE: Our overall finding was that abnormal behaviour was present in all sampled individuals across six independent groups of zoo-living chimpanzees, despite the differences between these groups in size, composition, housing, etc. We found substantial variation between individuals in the frequency and duration of abnormal behaviour, but all individuals engaged in at least some abnormal behaviour and variation across individuals could not be explained by sex, age, rearing history or background (defined as prior housing conditions). Our data support a conclusion that, while most behaviour of zoo-living chimpanzees is 'normal' in that it is typical of their wild counterparts, abnormal behaviour is endemic in this population despite enrichment efforts. We suggest there is an urgent need to understand how the chimpanzee mind copes with captivity, an issue with both scientific and welfare implications.